Behavioral Ecology Vol. 14 No. 6: 897–901
DOI: 10.1093/beheco/arg078
Conspecifics enhance egg production in
an egg-carrying bug
Mari Katvala and Arja Kaitala
Department of Biology, Box 3000, University of Oulu, Oulu FIN-90014, Finland
Variation in host availability and quality is likely to affect female decision making on when to lay eggs in arthropods. In the
present study, we show a case in which female reproduction is limited by the availability of conspecifics in a species in which
females preferably oviposit on conspecific bodies. Female golden egg bugs (Phyllomorpha laciniata; Heteroptera, Coreidae)
deposit eggs mainly on the bodies of both male and female conspecifics. Bugs other than parents carry most eggs. Egg carrying is
costly for individuals. A few eggs are laid on the bug’s food plant, but in most habitats, those eggs do not survive owing to
intensive ant predation. We explored if conspecific presence affects female egg production (eggs laid and eggs in reproductive
tract) in the field. In our experiment, conspecific presence (two females enclosed with food plant) increased female egg-laying
rate and egg production compared with that of females that were alone with the food plant. In nature, gaining a conspecific host
is difficult, and the encounter rate of conspecifics (i.e., operational host density) is likely to be important for female
reproduction. There are opposing interests between an egg-laying female and the recipient (male or female) because most eggs
are dumped on individuals that are not the parent of the eggs. Key words: conspecific dependence, egg-laying, female
reproduction, golden egg bug, social interactions. [Behav Ecol 14:897–901 (2003)]
n egg-laying arthropods, host availability and host quality
may vary both in space and time and may set boundaries for
female decision making on when, where, and how many eggs
to lay (for reviews, see Mangel, 1987; Minkenberg et al., 1992;
Thompson and Pellmyr, 1991). In addition, social facilitation,
which is an individual’s response to the presence of conspecifics (Vernon, 1995), may influence the reproductive
behavior of invertebrate species. For example, in the presence
of conspecifics, some simultaneous hermaphrodite fresh
water snails lay more eggs than when reared alone (Balea
perversa; Baur and Baur, 2000; Biophalaria glabata, Vernon,
1995). Also, ovipositionally naı̈ve females of Mediterranean
fruit fly (Ceratitis capitata) initiate ovipositor boring to the fruit
when the fruit is already occupied by a conspecific female
(Prokopy and Duan, 1998). Conspecific presence is also
important in species such as giant water bugs (Belostomatinae) in which females lay eggs on male bodies (Smith, 1997).
In these species, availability of males limits female reproduction (Ichikawa, 1989). We expect this to be the case in the
golden egg bug (Phyllomorpha laciniata, Vill, Heteroptera,
Coreidae) as well.
Female golden egg bugs dump eggs mainly on the bodies of
conspecific males and females. Occasionally, a few eggs are
laid on their food plant (Paronychia sp., Polycarpea, Caryophyllaceae). In the field, however, workers of the predator ant
species Pheidole pallidula (Nylander) (Hymenoptera, Formicidae) that inhabits the same habitats as the bugs (Bernard
1968; Kaitala, 1996; Kaitala et al., 2000) have been observed
to detect and forage effectively on arthropod eggs (Du Merle
et al., 1978) and corpses (Retana et al., 1991), including
golden egg bugs and their eggs laid on plant (Kaitala, 1996;
Kaitala et al., 2000). Thus, survival of eggs laid on food plants
is likely to be poor (Kaitala, 1996). Golden egg bugs are
commonly not the parents to the eggs they carry (Kaitala and
Katvala, 2001). In the field, 87% of the eggs carried by males
I
are not fertilized by the carrier (Miettinen and Kaitala, 2000).
Also, females are unable to oviposit on themselves, and thus,
they never carry their own eggs. In this manipulative system
driven by egg-laying females (Kaitala and Katvala, 2001),
females increase their offspring survival by dumping eggs on
conspecifics.
A recent study suggests that female egg-laying rate is limited
by lack of conspecific hosts in nature because the reproductive tracts of females collected from the field contained more
mature eggs than do those of the females that had been
enclosed with conspecifics (Kaitala and Smith, 2002). The
number of eggs in reproductive tract indicates a female’s
potential to oviposit when encountering a conspecific (Katvala and Kaitala, 2001b). Normally one to three eggs are laid
in one oviposition bout (Kaitala and Miettinen, 1997). In the
study of Kaitala and Smith (2002), females stopped egg laying
within 2 days in the laboratory when they were enclosed alone
with the food plant. At present, it is unknown how females
distribute eggs in natural circumstances among conspecifics
and food plants, and if eggs are accumulated in the
reproductive tract when conspecifics are absent. In addition,
it is unknown if female egg production is induced by presence
of conspecifics. We define egg production as the sum of the
total number of eggs laid and the number of mature eggs in
female reproductive tract. We expect females to increase egg
survival by ovipositing mainly on other bugs when possible
and to decrease egg laying and egg production when
conspecific egg carriers are absent.
In the field, we studied how conspecific presence affects
female egg laying, accumulation of eggs to reproductive tract,
and egg production. This was done by enclosing females
alone, in pairs or by altering conspecific presence during the
experiment.
METHODS
Address correspondence to M. Katvala. E-mail: mari.katvala@
oulu.fi.
Received 20 May 2002; revised 12 December 2002; accepted 2
February 2003.
2003 International Society for Behavioral Ecology
Natural history of the golden egg bug
The golden egg bug lives in the Mediterranean area and is
mainly found on dry sandy meadows with low vegetation,
including food plant of the species in high abundance
( Jeannel, 1909; Kaitala, 1996; Reuter, 1909). Bugs are found
Behavioral Ecology Vol. 14 No. 6
898
singly or in small groups of two or three individuals on the
inhabited area during reproductive season (Katvala M and
Kaitala A, unpublished data). The bugs are univoltine in
northern Spain but have a (partial) second generation in
southern Spain (Kaitala A, Katvala M, and Amat JA, unpublished data). They overwinter as adults and start to
reproduce in the following spring. Males receive nonpaternal
eggs during courtship (Kaitala, 1998; Kaitala and Miettinen,
1997; Katvala and Kaitala, 2001b). Also, males and females
receive eggs when in copula (Kaitala, 1996; Katvala and
Kaitala, 2001b) because a pair cannot resist egg laying by
a foreign female. Eggs dumped on a conspecific body are
carried passively until they hatch, normally after about 2 weeks
(Kaitala 1999). After hatching, the larvae independently move
to feed on the food plant. In the field, females carry on
average 2.5 eggs (range ¼ 1–14, n ¼ 378), and males an
average 5.5 eggs (range ¼ 1–28, n ¼ 440) in the middle of the
reproductive season (Kaitala, 1996). Females mate repeatedly
with different males. Copulations last often more than 20 h
(Kaitala and Miettinen, 1997). There may be an interval of
hours or days between copulation and egg laying (Kaitala and
Miettinen, 1997), and females are able to lay fertile eggs for
more than a month after copulation (Kaitala A, unpublished
data). Acceptance of eggs by the male during courtship does
not guarantee a copulation (Katvala and Kaitala, 2001b).
Field experiment
The experiment was carried out in the bug’s native habitat in
southern Spain near the city of El Puerto de Santa Maria. The
habitat was a sandy meadow with large bushes of Retama spp.
and lower vegetation, including plenty of Paronychia spp (see
Katvala and Kaitala, 2001a). Reproductively active females
were collected from open patches around the study site
because females close to oviposition prefer low vegetation
areas (Kaitala A, Katvala M, Ponsiluoma K and Amat JA,
unpublished data). Captured females were individually
marked with a paint tip. We also measured body length (see
Katvala and Kaitala, 2001b), and gently removed all the eggs
that the females carried. Females were kept separately in small
vials stored in a cool box (15 C) to avoid egg laying before the
experiment.
We enclosed one or two females in a netbag (20 3 25 cm;
female length is about 1 cm) that was tied on a sprig of food
plant that was naturally growing on our study site. The
experiment lasted 6 days. We altered conspecific presence
after 3 days in half of the netbags. The first 3 days is referred
as period 1; the last 3 days, as period 2. The four treatments
were as follows: (1) 3 days (period 1) alone fi 3 days (period
2) alone; (2) 3 days (period 1) paired fi 3 days (period 2)
paired; (3) 3 days (period 1) paired fi 3 days (period 2)
alone; and (4) 3 days (period 1) alone fi 3 days (period 2)
paired.
The netbag was bound to a living sprig of food plant to
allow female(s) a continuous access to fresh food and
a possibility to lay eggs on the plant. We had 26 females in
all treatments. Female body size did not differ statistically
among the four treatments (one-way ANOVA, F3,100 ¼ 0.525,
p ¼ .666). When females were paired, both females were
approximately similar in body size. Netbags were used to
reduce the interference of predators (ants and birds) and
nonexperimental conspecifics (egg-laying females and males).
However, we were unable to prevent other bugs or predators
from coming close to the netbags. Five females died during
period 2 because ants invaded their netbags; those individuals
were discarded from the analyses. After period 1, we replaced
all netbags to a new food plant sprig.
The number of eggs laid by females on a conspecific body
or on food plant was counted after both periods. After period
1, we left the eggs carried by each female on their backs. Some
eggs were also laid on the netbag, and the number of these
eggs was added to the number of eggs laid on the plant. After
the experiment, females were dissected to count the number
of mature eggs in reproductive tracts.
Statistical analyses
When females were paired, we added the eggs laid on food
plant to the number of eggs laid on a conspecific when
exploring the total number of eggs laid and eggs produced.
The mother of the eggs on plant was unknown, and thus, we
divided the number of eggs laid on the plant equally between
the two females and added that to the total number of eggs
laid on the conspecific for both females after both periods. In
paired netbags, both females were included in the data.
To explore female’s ability to regulate egg laying according
to conspecific presence among treatments, we counted the
difference between the number of eggs laid in period 1 and
period 2 for each female. By using the difference, we were
able to compare among treatments when the eggs were laid.
To analyze the differences in the egg laying among treatments, we used one-way ANOVA and Tukey HSD post hoc test.
To study whether conspecific presence affected accumulation of mature eggs to reproductive tract, we compared the
number of the eggs in reproductive tract among treatments.
The analysis was performed with one-way ANOVA and Tukey
HSD post hoc test. The dependent variable was square root–
transformed because the original data were not normally
distributed.
To explore females’ long-term response to the presence of
a conspecific, we compared the number of eggs produced
during the experiment. Egg production was defined as the
sum of the total number of eggs laid and the number of
mature eggs in female reproductive tract. The comparison was
performed between females enclosed alone (treatment 1) and
paired females (treatment 2) because in those treatments we
did not alter conspecific presence during the experiment. We
used the Mann-Whitney U test to test for significance of the
differences between the treatments because the dates were
not normally distributed.
RESULTS
The total number of eggs produced
Total egg production was examined by adding up the number
of eggs laid and the number of eggs in female reproductive
tract. Paired females (treatment 2) produced significantly
more eggs (mean 6 SE ¼ 8.44 6 0.86) than did females alone
(treatment 1) during the experiment (5.92 6 0.48; MannWhitney U test: U23,24 ¼ 156.5, p , .011) (Figure 1). Paired
females laid 6.39 6 0.67 eggs; females left alone, 2.63 6 0.35
eggs (Figure 2). Females that were able to choose whether to
lay eggs on a conspecific or on the food plant laid 96.8% of
their eggs (n ¼ 379 eggs, 78 females) on a conspecific body.
Egg laying among and within treatments
We used the difference between the number of eggs laid in
period 1 and period 2 for each female to study female egg
laying with respect to conspecific presence. To sum up Table
1, females laid eggs mainly when a conspecific female was
present, and they postponed egg laying when they were
enclosed alone (one-way ANOVA: F3,95 ¼ 31.4, p , .001)
(Figure 2 and Table 1). In treatment 1, in which females were
Katvala and Kaitala • Conspecifics and egg production
Figure 1
The number of eggs produced (mean 6 SE) in the field experiment.
Filled bars represent the number of eggs laid during periods 1 and 2,
and open bars represent the number of mature eggs in female
reproductive tract. The treatment in period 2 is printed in bold.
Sample sizes are 24, 24, 26, and 26 females, respectively.
alone all the time, they maintained a low egg-laying rate
during the experiment (Figure 2 and Table 1). Paired females
of treatment 2 continued egg laying during both periods.
Individual females were able to respond to the change in
conspecific presence. In treatments 3 and 4, in which the
conspecific presence was altered between periods, eggs were
laid mainly when females were paired and not when females
were alone, independently on the order of being paired
(Figure 2 and Table 1).
Eggs in female reproductive tract
Dissected females had zero to 10 eggs in their reproductive
tract, and the number of eggs differed among treatments
(one-way ANOVA: F3,95 ¼ 4.82, p ¼ .004). Two subsets stand
out in Figure 1 (see white bars), depending on whether the
females were paired or alone during the last or both periods.
Females of treatment 3 (paired fi alone) had more eggs in
their reproductive tract (3.54 6 0.42) than did females of
treatments 2 (2.04 6 0.32; paired fi paired; Tukey HSD:
mean difference ¼ 0.38, SE ¼ 0.14, p ¼ .035) and 4 (2.04 6
0.21; alone fi paired; Tukey HSD: mean difference ¼ 0.42,
SE ¼ 0.14, p ¼ .018), in which females were paired during period 2. Females of treatment 1 (alone fi alone) also had more
eggs in reproductive tract (3.29 6 0.41) than did females
of treatment 2 (2.04 6 0.32; paired fi paired), but the
difference was not quite significant (Tukey HSD: mean
difference ¼ 0.372, SE ¼ 0.144, p ¼ .055). The difference
between females of treatment 1 (3.29 6 0.41; alone fi alone)
and females of treatment 4 (2.04 6 0.21; alone fi paired) was
not statistically significant (Tukey HSD: mean difference ¼
0.324, SE ¼ 0.14, p ¼ .101), even though the females in
treatment 1 have an average of almost 1.3 eggs more in the
reproductive tract than did females of the treatment 4.
However, these results indicate that conspecific presence
during the last period affected the number of eggs females
had in their reproductive tract.
DISCUSSION
Egg production, defined as the sum of the total number of
eggs laid and the number of mature eggs in the female
reproductive tract of paired females, was significantly higher
899
Figure 2
The cumulative number of eggs laid (mean 6 SE) by females in the
field experiment. On the x-axis is the number of days from the
beginning, after which the number of eggs has been counted, the
origin is the time when the experiment was started. During period 1,
sample sizes are 26 females in each treatment; during period 2,
sample sizes are 24, 24, 26, and 26 females, respectively.
than that of the females that were alone during the
experiment. Females did not use food plants as an alternative
host in the absence of conspecifics but postponed egg laying
while alone, which resulted in mature eggs accumulating in
the female reproductive tract. Females quickly adjusted their
egg production to the presence of a conspecific, and they soon
resumed laying eggs when having access to a conspecific bug.
Female dependence on conspecifics
The number of eggs laid and egg production were higher
when a conspecific was present as potential egg carrier than
when a female was alone. When possible, almost all eggs
(96.8%) were dumped on another female. In treatments 3
and 4, in which conspecific presence was altered during the
experiment, females increased or decreased the number of
eggs laid depending on whether a conspecific was present or
not. They postponed oviposition when they were alone, and
then mature eggs accumulated in the reproductive tract.
These results emphasize the importance of other bugs for an
egg-laying female and their dependence on conspecifics.
Further, these results indicate a female’s ability to respond
and to adjust egg laying to conspecific presence in short-term
perspective. In addition to an earlier study (Kaitala and Smith,
2002), this shows that females clearly prefer to oviposit on
a conspecific back and wait for an opportunity to do so. Lack
of sperm is an unlikely explanation for decreased number of
eggs laid because after isolation females resumed egg laying
(treatment 4, see Figure 2). In a previous laboratory
experiment, the number of eggs laid during the experiment
was unaffected by the presence or absence of males (Kaitala
and Smith, 2002).
The golden egg bug is an example of social facilitation in
a broad sense because conspecific presence affects female egg
laying and egg production. However, the golden egg bug
differs from the other invertebrates studied in this context
(e.g., fresh water snails; Baur and Baur, 2000, Vernon, 1995)
because eggs are laid on conspecifics. Therefore, to find out
the proximate stimulus that induces egg production, one
should perform an experiment in which the social factor can
be separated from egg laying on conspecifics’ backs. This can
be performed, for example, by enclosing a female solitary in
an netbag and placing it in an enclosure in which bug(s) are
present. However, egg-laying rate of the bug is low. In our
Behavioral Ecology Vol. 14 No. 6
900
Table 1
Directions of the differences for the number of eggs laid between
periods 1 and 2
Treatment
1.
2.
3.
4.
Alone fi alone
Paired fi paired
Paired fi alone
Alone fi paired
Direction of the
difference between
the periods
1
1
1
1
»2
.2
.2
,2
N
Differs significantly
from the treatments*
24
23
26
26
2,
1,
1,
1,
3, 4
4
4
2, 3
The significant differences in the one-way ANOVA among the
treatments in the field experiment are indicated. As a dependent
variable, we used the difference of the number of eggs laid between
periods.
* One-way ANOVA, difference between treatments in the Tukey HSD
post hoc test is significant at the .05 level.
6-day field experiment, paired females laid 6.39 6 0.67 eggs
(mean 6 SE; treatment 2), which is in concert with earlier
results (Kaitala and Miettinen, 1997). Eggs in this species are
large; one egg equals 4% of a male’s body weight and 1.2–
2.0% of a female’s body weight (Miettinen M, Katvala M, and
Kaitala A, unpublished data). Roughly, females produce one
egg per day during their reproductive period.
Egg laying of the golden egg bug is comparable to
Belostomatinae giant water bugs (Smith, 1997) and pipefishes
(Berglund et al., 1989), with exclusive paternal care in which
female reproduction depends on the availability of free space
on males’ backs (Ichikawa, 1989) or in males’ body cavity
(Berglund et al., 1989). Crucial differences to these species
are that female bugs lay eggs on both male and female
conspecifics, and egg laying on male backs often occurs
without copulation (Katvala and Kaitala, 2001b). Space on the
back of conspecifics is not a limiting factor for egg-laying
females because bugs seem to be accepted as hosts independently on the number of eggs they already carry
(Kaitala, 1998). In natural populations, male bugs carry on
average six eggs, and we have seen a male carrying up to 28
eggs (Kaitala, 1996). Operational host density (see below)
seems to be more crucial factor for an egg-laying female than
is space on conspecifics’ backs.
Kaitala and Smith (2002) suggested that females have
difficulties to gain conspecific hosts in the field, and females
actively search for conspecific bugs for egg laying (Kaitala A,
Katvala M, Ponsiluoma K, and Amat JA, unpublished data).
Gaining a conspecific host is difficult because egg carrying
seems not to be voluntary and bugs resist receiving eggs if
possible (see Kaitala and Miettinen, 1997). The number of
available conspecifics and encounter rate of bugs, that is,
operational host density, may affect female egg production.
Courting males and mating pairs can be considered as
potential hosts, whereas females that have recently oviposited
are not available because they seem to hide (Kaitala A, Katvala
M, Ponsiluoma K, and Amat JA, unpublished data). Whether
female egg production is affected by operational host density
in natural circumstances remains to be studied.
Eggs laid on food plant
Considerably fewer eggs were laid on food plants than on
conspecific bodies during the experiment. In the presence of
a conspecific, only 3.2% of the eggs was laid on food plant. It
is unknown if those eggs were laid on plants owing to an
inability to terminate an interrupted oviposition attempt on
a conspecific body on purpose, or whether a female had seen
a bug outside the net and started egg laying. It remains to be
seen if the threshold to lay eggs on food plants decreases with
increasing female age or decreasing conspecific density (see
Minkenberg et al., 1992). Because potential carriers are able
to interrupt an oviposition attempt, it is likely that females
close to oviposition occasionally have to accept to lay the egg
that is about to be laid on a food plant.
Females in the present study did not flexibly alternate
laying eggs between conspecifics and food plants. Different
egg laying behavior has been reported from another P.
laciniata population. In a mountainous Sicilian population in
Italy, females are known to lay eggs mainly on plants (Mineo,
1984). However, in this area Paronychia sp., which is used by
the Spanish populations, is absent, and so the Sicilian bugs
use other host plants (Mineo, 1984). Intraspecific variation
among populations in host preferences has been reported, for
example, in some butterflies (see Janz and Nylin, 1997). It
would be interesting to study the factors affecting female
oviposition preference and variation in life-history traits
among populations preferring different hosts.
To conclude, in the golden egg bug female egg laying and
egg production are dependent on interactions with conspecifics. However, interests of the egg-laying female and egg
recipients are often contradictory because most eggs are
dumped on non-parental bugs.
We thank J.A. Amat, K. Ponsiluoma, and K. Kangas for field assistance.
J.T. Forsman, R. Härdling, and the Evolutionary Ecology Discussion
Group at the department gave constructive criticism to the earlier
drafts of the manuscript. The study was supported by the Academy of
Finland (project 53899).
REFERENCES
Baur B, Baur A, 2000. Social facilitation affects longevity and lifetime
reproductive success in a self-fertilizing land snail. Oikos 88:612–
620.
Berglund A, Rosenqvist G, Svensson I, 1989. Reproductive success
of females limited by males in two pipefish species. Am Nat 133:
506–516.
Bernard F, 1968. Faune de l’Europe et du Bassin Méditerranéen 3. Les
fourmis (Hymenoptera Formicidae) d’Europe occidentale et
septentrionale. Masson et Cie, Paris.
Du Merle P, Jourdheuil P, Marro JP, Mazet R, 1978. Évolution
saisonnière de la myrmécofaune et de son activité prédatrice dans
un milieu forestier: les interactions clairière-lisière-forèt. Ann Soc
Ent France 14:141–157.
Ichikawa N, 1989. Breeding strategy of the male brooding water bug,
Diplonychus major esaki (Heteroptera: Belostomatidae). J Ethol
7:133–140.
Janz N, Nylin S, 1997. The role of female search behaviour in
determining host plant range in plant feeding insects: a test of
the information processing hypothesis. Proc R Soc Lond B 264:
701–707.
Jeannel R, 1909. Sur les murs et les métamorphoses de Phyllomorpha
laciniata Vill (Hem. Coreidae). Bull Soc Entomol France 15:282–
286.
Kaitala A, 1996. Oviposition on the back of conspecifics: an unusual
reproductive tactic in a coreid bug. Oikos 77:381–389.
Kaitala A, 1998. Is egg carrying attractive? Mate choice in the golden
egg bug (Coreidae, Heteroptera). Proc R Soc Lond B 265:779–783.
Kaitala A, 1999. Counterstrategy to egg dumping in a coreid bug:
recipient individuals discard eggs from their backs. J Insect Behav
12:225–232.
Kaitala A, Espadaler X, Lehtonen R, 2000. Ant predation and the cost
of egg carrying in the golden egg bug: experiments in the field.
Oikos 89:254–258.
Kaitala A, Katvala M, 2001. Sexual interactions and conspecific
exploitation in an egg-carrying bug. Ann Zool Fennici 38:215–221.
Kaitala A, Miettinen M, 1997. Female egg dumping and the effect
of sex ratio on male egg carrying in a coreid bug. Behav Ecol 8:
429–432.
Katvala and Kaitala • Conspecifics and egg production
Kaitala A, Smith RL, 2002. Do golden egg bugs (Phyllomorpha
laciniata: Heteroptera, Coreidae) require conspecifics for oviposition? J Insect Behav 15:171–180.
Katvala M, Kaitala A, 2001a. Egg performance on an egg-carrying bug:
experiments in the field. Oikos 93:188–193.
Katvala M, Kaitala A, 2001b. Male choice for female current fecundity
in an polyandrous egg carrying bug. Anim Behav 62:133–137.
Mangel M, 1987. Oviposition site and clutch size in insects. J Math
Biol 25:1–22.
Miettinen M, Kaitala A, 2000. Copulation not a prerequisite to male
reception of eggs in the golden egg bug Phyllomorpa laciniata
(Coreidae; Heteroptera). J Insect Behav 13:731–740.
Mineo G, 1984. Notizie biologiche su Phyllomorpha laciniata (Vill.)
(Rhynchota, Het., Coreidae). Phytophaga 2:117–132.
Minkenberg OPJM, Tatar M, Rosenheim JA, 1992. Egg load as a major
source of variability in insect foraging and oviposition behaviour.
Oikos 65:134–142.
901
Prokopy RJ, Duan JJ, 1998. Socially facilitated egg laying in
Mediterranean fruit flies. Behav Ecol Sociobiol 42:117–122.
Retana J, Cerdá X, Espadaler X, 1991. Arthropod corpses in
a temperate grassland: a limited supply? Holarct Ecol 14:63–67.
Reuter MO, 1909. Quelques mots sur les Phyllomorphes (Hem.
Coreidae). Bull Soc Entomol France 15:264–268.
Smith RL, 1997. Evolution of paternal care in the giant water bugs
(Heteroptera: Belostomatidae). In: Social behavior in insects and
arachnids (Choe JC, Crespi BJ, eds). Cambridge: Cambridge
University Press; 116–149.
Thompson JN, Pellmyr O, 1991. Evolution of oviposition behavior
and host preference in lepidoptera. Annu Rev Entomol 36:
65–89.
Vernon JG, 1995. Low reproductive output of isolated self-fertilizing
snails: inbreeding depression or absence of social facilitation? Proc
R Soc Lond B 259:131–136.